Recent progress in understanding mammalian color vision
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Ophthal. Physiol. Opt. 2010 30: 422–434
The Verriest Lecture 2009
Recent progress in understanding mammalian
color vision
Gerald H. Jacobs
Department of Psychology and Neuroscience Research Institute, University of California, Santa
Barbara, CA 93106, USA
Abstract
There have been significant advances in our understanding of mammalian color vision over the past
15 years. This paper reviews a number of topics that have been central to these recent efforts,
including: (1) the extent and nature of ultraviolet vision in mammals, (2) the evolutionary loss of short-
wavelength-sensitive cones in some mammals, (3) the possible roles of rod signals in mammalian
color vision, (4) the evolution of mammalian color vision, and (5) recent laboratory investigations of
animal color vision. Successes in linking opsin genes and photopigments to color vision have been
key to the progress made on each of these issues.
Keywords: evolution of color vision, mammalian color vision, opsin genes, photopigments,
ultraviolet vision
Mammals were traditionally believed to constitute
Introduction
significant exceptions to this picture. In his classic
Results obtained from comparative studies of retinas, treatise on vertebrate eyes, Gordon Walls encapsulated
and inferences drawn from opsin gene phylogenies, that idea by noting that, although primates stand as a
show that at an early stage in vertebrate history, almost clear exception, ÔWithin the mammals color vision is by
certainly by the time jawless and jawed vertebrates no means widespreadÕ (Walls, 1942). Over the next
diverged (540 million years ago (mya)), our ancestors 50 years this idea was echoed on numerous occasions by
had already evolved four classes of cone photopigment other writers. WallsÕ explanation for the elaborate color
and so possessed the photopigment basis for color vision vision detected in most contemporary vertebrate groups,
(Collin et al., 2009). Shortly thereafter, colored oil and the simplified nature (or, indeed, complete absence)
droplets, another retinal appurtenance usually associ- of a color vision capacity in most mammals, was that it
ated with complex color vision, also appeared (Robin- simply reflected the early history of mammals when they
son, 1994). Three or four classes of cone pigment are had undergone a long period of predominant noctur-
present in many contemporary representatives from four nality, and as a consequence had largely abandoned the
of the major vertebrate groups (fishes, birds, amphibians machinery required to support many quintessential
and reptiles) while colored oil droplets are found in daylight visual capacities, including color vision. In an
numerous members of the latter three groups (Bow- earlier review of the literature on mammalian color
maker, 1991, 2008): thus, to varying degrees, many vision I concluded that, counter to the conclusions of
vertebrates probably maintained a capacity for elabo- Walls and his followers, the presence of color vision, at
rate color vision over the long sweep of their histories. least as it is technically defined, is actually quite
widespread among contemporary mammals and that
cones, rather than having sometimes been lost and
Received: 10 September 2009 subsequently regained as Walls had surmised, were most
Revised form: 18 December 2009 likely carried forward over the unbroken sweep of
Accepted: 25 December 2009 mammalian history (Jacobs, 1993). The years since that
Correspondence and reprint requests to: Gerald H. Jacobs.
review have witnessed considerable further progress
Tel.: 805 893 2446; Fax: 805 893 4303. towards understanding mammalian color vision. Here
E-mail address: jacobs@psych.ucsb.edu I comment on several topics having to do with
doi: 10.1111/j.1475-1313.2010.00719.x ª 2010 The Author, Ophthalmic and Physiological Optics ª 2010 The College of OptometristsThe Verriest Lecture: G. H. Jacobs 423
mammalian color vision that have come to the fore vision is common and much studied, it appears that UV
during this period. sensitivity can be useful in both mate choice and
foraging, among other activities, although it is unclear
if avian UV vision actually evolved to subserve these
Ultraviolet vision in mammals
purposes (Church et al., 2001; Hart and Hunt, 2007).
It has long been known that many terrestrial arthropods Thus far there is no evidence that mammalian UV vision
have high sensitivity to ultraviolet (UV) light (Jacobs, can be employed to achieve similar goals; indeed, there
1992; Goldsmith, 1994). Detection of similar mecha- are some indications to the contrary: for instance, an
nisms in vertebrates is more recent, but even as these explicit laboratory test of foraging in house mice found
were eventually established in various birds, fishes, that these rodents were indifferent to the presence or
reptiles and amphibians, it was still supposed that absence of UV-linked cues (Honkavaara et al., 2008).
mammals were insensitive to UV, a conclusion princi- An alternative possibility has come from the observation
pally based on the mistaken idea that the lenses of all that the urine of some rodent species has high reflectivity
mammalian eyes have low transmissivity to short- to UV (Viitala et al., 1995), suggesting that in such
wavelength light (Goldsmith, 1990). That changed with animals scent marking with urine might utilize a UV-
the discovery that the retinas of several common species sensitive communication channel (Chavez et al., 2003).
of rodent (including mice, rats, gerbils and gophers) in Whether that is true or not remains to be seen, but it is
fact contain a separate spectral mechanism with max- noteworthy that high reflectivity is not characteristic of
imal sensitivity in the UV (Jacobs et al., 1991). This the urine of many mammals, even those known to have
claim was contested (Soucy et al., 1998), but subsequent UV cones, e. g., the house mouse (Kellie et al., 2004).
electrophysiological (Lyubarsky et al., 1999), spectro- An additional point of concern is that most of the
photometric (Yokoyama et al., 1998), and behavioral species so far known to have UV cones are nocturnal,
measurements (Jacobs et al., 2001), have all verified the thus being predominantly active during a phase of the
presence of cones containing UV pigment in rodent illumination cycle when UV light is not naturally very
retinas. Although it is not the predominant arrangement abundant (Johnsen et al., 2004). Finally, it has been
among mammals, UV cones have subsequently been suggested that natural fluctuations in UV light probably
detected in a number of other rodent species (Peichl, play only a limited role in the entrainment of mamma-
2005) as well as in several species of bat (Wang et al., lian circadian systems (Hut et al., 2000). In summary,
2004; Muller et al., 2009; Zhao et al., 2009) and some although laboratory tests of mammals with UV cones
marsupials (Strachan et al., 2004; Arrese et al., 2005; show clearly that they are capable of exploiting signals
Hunt et al., 2009b). There are almost certainly other from these receptors to guide behavioral choices under
mammalian species so far unstudied that also possess photopic test conditions (Jacobs et al., 2003, 2004) we
UV cones. still have little idea of how this capacity may be
A better understanding of the origin of UV cones in employed naturally.
mammals has emerged from recent molecular genetic
studies of photopigment opsin genes. All vertebrate cone
Evolutionary loss of SWS1 cones
pigments having maximum sensitivity (kmax) in the short
wavelengths (360 nm to 440 nm) are specified by genes As noted, the photopigments of all mammalian short-
from one (SWS1) of the four cone-opsin gene families wavelength-sensitive cones are specified by opsin genes
(Bowmaker, 2008). Cross-species comparisons of the drawn from the SWS1 family. Some years ago studies
residues implicated in the spectral tuning of the SWS1 involving both opsin immunolabelling (Wikler and
cone opsins suggest that the ancestral mammalian SWS1 Rakic, 1990), and behavioral and electrophysiological
pigment was in fact a UV pigment (Hunt et al., 2001). In measurements (Jacobs et al., 1993; Deegan and Jacobs,
many mammalian lineages the occurrence of a small 1996), failed to detect functional short-wavelength-
number of amino acid substitutions subsequently shifted sensitive cones in the retinas of two species of nocturnal
the kmax of the cone pigment from the UV to a variety of primates—the anthropoid Aotus (owl monkey) and the
locations in the visible spectrum (Yokoyama, 2009). strepsirrhine Otolemur (bushbaby). A subsequent genet-
Evolutionary changes of this kind, though common, ic examination revealed that the absence of S cones in
have not been universal; in particular, the mammalian these primates results from mutational changes in the
species noted above have all retained the ancestral S-cone opsin genes that render them incapable of
mammalian short-wavelength pigment. expressing opsin protein, i. e., they had become pseud-
Why have some mammals retained their UV cones ogenes (Jacobs et al., 1996b). Since these two primates
while others have not? Answering that question would are only distantly related, and since the structural nature
be easier if we understood the relative values and costs of their SWS1 gene defects differed, it seemed likely that
of UV vision for mammals. In diurnal birds, where UV the conversions of the SWS1 genes to pseudogene status
ª 2010 The Author, Ophthalmic and Physiological Optics ª 2010 The College of Optometrists424 Ophthal. Physiol. Opt. 2010 30: No. 5
must have occurred independently in the two lineages. Can similar functional explanations account for the
Further, because both of these species are nocturnal it presence of mammalian S-opsin pseudogenes? In most
seemed plausible to assume there must be other noctur- mammalian retinas SWS1-specified cones are infrequent
nal mammals in whom gene mutations had also relative to the numbers of LWS-specified cones, typi-
rendered their S-cone pigments nonfunctional (Jacobs cally making up no more than 10% of the total cone
et al., 1996b). complement. Because of their relative sparsity, as well as
This latter prediction has been amply borne out. limitations imposed by the optics of mammalian eyes, S
Scattered species from four orders of eutherian mam- cones make little contribution to total photon capture
mals (various rodents, primates, cetaceans, and carni- and they support significantly lower spatial and tempo-
vores) similarly lack functional S cones, and in cases ral resolution than do the more abundant long wave-
where it has been examined, their absence can be length cones (Calkins, 2001). Rather, the principal role
traced to corresponding opsin gene defects (Jacobs, subserved by mammalian S cones is to generate a signal
2009). Photic activity classifications are imprecise, but that can be contrasted to that derived from stimulation
all the mammals so far found to lack S cones are of longer wavelength cones, with the combination thus
principally nocturnal, as were the primates in whom providing the basis for a dimension of color vision. Since
S-opsin pseudogenes were first detected. Supporting the most mammals have only a single type of LWS cone, the
possibility of a causal link between pigment loss and loss of viable S cones eliminates the possibility of any
photic activity cycle, is the observation that while most cone-based color vision, and that is just what has
of the carnivore procyonids are nocturnal, and of these happened in those species in which the SWS1 genes have
both Procyon (the raccoons) and Potos (kinkajous) become pseudogenes.
lack short-wavelength cones, a closely-related procyo- What values and costs might be associated with
nid (Nasua, the coati) is diurnal and retains functional abandoning a dimension of color vision? If animals are
S cones (Jacobs and Deegan, 1992). Although it seems nocturnal, as at least most of these species seem to be,
that nocturnality sets the stage for SWS1 cone opsin then they would normally be behaviorally active when
genes to become pseudogenes, that feature cannot be ambient light levels are insufficient to support cone-
the sole issue since many nocturnal mammals retain a based vision and thus color vision in such animals would
full complement of functional short-wavelength cones, seem at first glance to offer minimal advantage. On the
e.g., rats and mice. There are also the extreme other hand, many contemporary mammals classified as
examples offered by some subterranean mammals, nocturnal are also active at dawn and dusk (Macdonald,
animals that lead lives almost completely devoid of 2001), times when illumination conditions could well
light exposure yet still retain fully functional short- support some role for cone vision. In addition, even the
wavelength sensitive cones (Peichl et al., 2004; Williams most resolutely nocturnal species occasionally awaken
et al., 2005). Finally, if a nocturnal lifestyle promotes and become active during daylight hours in order to
the pseudogenization of SWS1 opsin genes it is curious initiate behaviors for which color vision might prove
why this did not happen in widespread fashion during useful; for instance, to escape predation, to respond to
the long period in their early history when mammals weather contingencies, or to initiate foraging driven by
were principally nocturnal. the stress of food scarcity (Bearder et al., 2006). If there
In recent years pseudogenes associated with receptor seems to be at least some potential value in retaining
operation have been discovered in other sensory sys- color vision in a nominally nocturnal species, then
tems; for example, within families of olfactory (Gilad perhaps one should look instead to the debit side of
et al., 2004), pheromone (Zhang and Webb, 2003), and maintaining color vision. Energy efficiency has been
gustatory (Go et al., 2005) receptor genes. A common shown to act as a strong selective force in brain
suggestion is that the transition of genes to pseudogenes evolution (Niven and Laughlin, 2008) and conceivably
occurs when the function(s) they support become that issue is at play here. Although there seems no way
dispensable and, that being the case, this process and as yet of evaluating the possibility directly, the short-
its dependence on details of the interaction of organisms wavelength sensitive cones required to support a dimen-
with their environments may be particularly easy to sion of color vision are few in number, which would
observe in sensory systems (Go et al., 2005) One seem to minimize their metabolic expense. In summary,
possible example so cited is the large increase in the if there are any general adaptive reasons associated with
proportion of anthropoid olfactory receptor genes that the inactivation of mammalian SWS1 cone opsin genes,
are pseudogenes, relative to what is found in rodents. they are not yet apparent.
That difference is attributed to the lessened importance Among mammals so far studied, SWS opsin pseud-
of a keen sense of smell among the primates, perhaps ogenes seem sometimes to have emerged near the
occurring in exchange for their increased dependence on evolutionary base of the lineage and in other cases only
vision (Gilad et al., 2004). in the distal branches of the family. Among the latter
ª 2010 The Author, Ophthalmic and Physiological Optics ª 2010 The College of OptometristsThe Verriest Lecture: G. H. Jacobs 425
examples would be the procyonids, described above,
Rods and mammalian color vision
where fairly closely-related genera can have either
functional or non-functional S cone pigments. Perhaps Because rods and cones overlap in their operating
most striking among the former are the marine mam- ranges (in human vision by some 4 log units of
mals. A genetic survey of the SWS1 opsin genes in 16 intensity), and because the signals from these receptor
species of cetaceans identified mutational changes in all types share neural pathways into the central visual
of these species that should obviate the production of system, it has long been apparent that rod signals can
functional S-cone pigment (Levenson and Dizon, 2003). potentially influence cone-based vision. Among those
In fact, in one cetacean sub-order (the odontocetes) all demonstrated influences are cases where rod signals
the species share in common a mis-sense mutation in cause complex alterations in color appearance (Volbr-
their S-cone opsin genes implying that pseudogenes echt et al., 1995; Buck, 2004) and cases involving
must have been present prior to the time these animals viewing conditions (mesopic light levels, large test fields)
began to diverge in the Oligocene (25–38 mya). Further, where rod signals can be contrasted to signals derived
in support of earlier evidence derived from opsin from a single class of cones to yield novel color vision
immunolabelling (Peichl and Moutairou, 1998), a (Smith and Pokorny, 1977). The following examples
genetic survey found that all the pinnipeds (seals, sea illustrate that similar influences from rod signals on
lions, walrus) also have a gene-linked loss of S-cone color vision also operate in non-human mammals.
function (Levenson et al., 2006). The complete absence An early behavioral experiment conducted on a
of SWS1 cones in both of these two distinct mammalian strepsirrhine primate, the ring-tailed lemur (Lemur
orders raises the possibility that such a loss may have catta), included tests of spectral sensitivity and color
yielded some adaptive advantages. What those might be discrimination (Blakeslee and Jacobs, 1985). The latter
is unclear, although some suggestions have been offered provided evidence for the presence of some (relatively
(Peichl et al., 2001). Particularly puzzling in this regard feeble) color discrimination in the red-green portion of
is that present day cetaceans and pinnipeds occupy the spectrum; specifically, these animals were able to
distinctively different photic environments: the former make unique dichromatic color matches (540 nm +
strictly aquatic, often active in environments where 645 nm = 570 nm) with the match proportions signi-
photons are a scarce commodity; whereas pinnipeds are ficantly displaced in the protan direction relative to
amphibious inhabiting both aquatic and terrestrial those made by normal human trichromats. Since
habitats, the latter often characterized by high photopic subsequent results derived from both electrophysiolog-
light loads. ical measurements (Jacobs and Deegan, 1993, 2003),
Observations made on the owl monkey (Aotus) may and from an analysis of cone opsin genes (Tan and Li,
argue against expecting any simple relationships be- 1999), show that this species expresses only a single cone
tween photic environments and S-cone absence. Aotus is photopigment active in the middle to long-wavelength
a nocturnal monkey, but is believed to have evolved portion of the spectrum (with kmax of 545 nm), the
from diurnal ancestors some 12–15 mya (Setoguchi and color discriminations found in the earlier study must
Rosenberger, 1987). Several contemporary species of perforce have derived from the ability of these animals
Aotus share in common a mis-sense mutation which to jointly utilize rod and cone signals.
renders their S-cone opsin gene nonfunctional and this That case is not unique; for example, genetic exam-
implies that the pseudogene appeared early in the ination reveals that the pinniped California sea lion
history of the genus, perhaps not long after the (Zalophus californaus) has only a single cone type
transition to nocturnality (Levenson et al., 2007). (Levenson et al., 2006) yet it too seems capable of
Although most of the animals comprising modern Aotus making color discriminations that would be technically
have remained stringently nocturnal, one species, impossible without the exploitation of rod signals
A. azarae, is cathemeral, i.e., it is frequently behavior- (Griebel and Schmid, 1992). One important point to
ally active during daylight hours as well as at night be derived from these examples is that deductions about
(Fernandez-Duque, 2003). Despite the absence of func- color vision based solely on knowledge of the cone
tional S cones, and thus any possibility of a conven- complement, as for instance is commonly done follow-
tional color vision capacity, this monkey forages quite ing examination of cone opsin genes, will miss possible
successfully on colored fruits and tree flowers under influences from rod contributions. Such influences may
lighting conditions where its vision must be based on be particularly relevant for those many mammals that
signals from only a single type of cone pigment. If have heavily rod-dominated retinas because, as noted
nothing else, this example underlines the fact that we are above, such animals often display photic rhythms that
only at the beginning of understanding the extent and render them behaviorally active under illumination
practical implications of the gene-driven losses of S-cone conditions favorable for supporting joint rod and cone
that characterizes some mammals. contributions.
ª 2010 The Author, Ophthalmic and Physiological Optics ª 2010 The College of Optometrists426 Ophthal. Physiol. Opt. 2010 30: No. 5
Among the most noteworthy features of mammalian The schematic of Figure 2 suggests the evolutionary
retinas are the large species variations in rod/cone ratios fate of these four cone opsin gene families in mammals.
and in the pattern of distribution of cones in the retinal As for amphibians, cone opsin genes from the Rh2
mosaic (Ahnelt and Kolb, 2000). These variations will family are not found in any contemporary mammal
significantly impact the thresholds and dynamic ranges suggesting it was lost prior to the onset of mammalian
for rod and cone vision and they will influence the limits divergence. Contemporary monotremes (platypus and
of color discrimination. Both of these facts were earlier echidna) have photopigments from the SWS2 and LWS
taken to suggest that the relative rod/cone mix and their families and their genomes also contain a pseudogene
spatial distributions could be targets for selection in the from the SWS1 family (Davies et al., 2007). Genes
evolution of color vision (Jacobs, 1993). That idea begins drawn from the SWS2 family are not present in either
to seem more plausible in the face of recent research that marsupial (Strachan et al., 2004; Cowing et al., 2008) or
compared structural features of the visual cortex and the eutherian mammals and must, therefore, also have been
retina in a variety of nocturnal and diurnal mammals and lost prior to the divergence of these two lineages
showed that, indeed, relative rod and cone complements (Figure 2). Both of these lines retain viable representa-
are very sensitive to niche-specific selection pressures and tives from the SWS1 and LWS families. These various
that plasticity stands in striking contrast to the much gene losses are usually suggested to have occurred
greater conservatism of the size of central visual struc- during the long period of early mammalian nocturnality,
tures (Kaskan et al., 2005). The relative numbers of but exactly how that exposure may have fostered such a
retinal cell types can be readily altered through nothing loss is not known. Whatever the reason, the outcome
more elaborate than changes in the schedule of retinal has been to limit most animals in these groups to only
neurogenesis, and such schedule alterations could thus two types of cone pigment although, as noted below,
provide a proximate mechanism through which selection significant exceptions to this rule occur among primates.
might impact the relative influences of rods on mamma- Sequence comparisons of cone opsin genes from con-
lian color vision (Finlay, 2008). temporary eutherian mammals suggest that the SWS1
and LWS gene families provided ancestral eutherian
mammals with cone pigments having kmax values of
Evolution of color vision in mammals
360 nm and 560 nm (Hunt et al., 2001; Yokoyama
At the time of the 1993 review, a renewed interest in the
evolution of color vision was just beginning to manifest
itself. Triggered by a substantial accrual of information
about opsin genes, as well as by new examinations of the
ecology of color vision, much more has now been
learned about this. A number of reviews dealing with
various aspects of this topic have appeared in recent
years (for the most recent of these see Osorio and
Vorobyev, 2008; Collin et al., 2009; Hunt et al., 2009a;
Jacobs, 2009; Yokoyama, 2009) so I provide here only a
brief summary of the relevant findings.
Evolution of opsin genes
Phylogenetic analysis shows that all vertebrate photo-
pigments are specified by opsin genes belonging to five
families—four for the cone opsins, the other for rod
opsins (Yokoyama, 2000). Each of these gene families
produce opsins structured to yield photopigments that
cover the range of spectral peaks indicated in Figure 1 Figure 1. Spectral range of vertebrate photopigments. All vertebrate
(top). As a result of prior gene duplications, these cone photopigment opsins are specified by members of the five opsin
opsin gene families are believed to have already emerged gene families listed at the top. When combined with an 11-cis-retinal
at a point early in vertebrate history. Pigments drawn chromophore, variations in the gene sequences yield photopigments
whose kmax values cover the spectral ranges indicated by the
from each of the four cone opsin gene families are found
horizontal lines. Cone photopigments in eutherian mammals come
in various present-day birds, fishes, and reptiles. Rep- exclusively from the SWS1 and LWS families. The two ancestral
resentation from only three of these families (Rh2 is cone pigments found in these animals are believed to have had the
missing) has so far been detected among contemporary spectral absorption curves sketched at the bottom. (Modified from
amphibians (Bowmaker, 2008). Jacobs, 2009).
ª 2010 The Author, Ophthalmic and Physiological Optics ª 2010 The College of OptometristsThe Verriest Lecture: G. H. Jacobs 427
all the naturally observed variations (Neitz et al., 1991;
Carroll and Jacobs, 2008). A similarly small number of
amino acid substitutions are linked to variations in the
mammalian photopigments specified by the SWS1 genes
(Hunt et al., 2004).
Although interactions between environmental signals
and sensory capacities impacting evolution can be
complex (Endler, 1992), one common assumption is
that the spectral positioning and number of cone
pigment types that evolve reflect those best adapted to
support the visual tasks requisite for survival (Lythgoe
and Partridge, 1989). In contemporary mammals pig-
ments from the LWS family span a range of spectral
positions having kmax values from 500 to 560 nm. If,
as believed (above), the spectral location of the ancestral
LWS pigment was close to the latter location, there must
have been numerous shifts in the spectral position of this
pigment toward the shorter wavelengths. Most euthe-
rian mammals also have an SWS1 cone pigment.
Figure 2. Suggested fate of the four cone opsin gene families during Through an analysis of a collection of natural images
mammalian evolution. The range of photopigment absorption prop- viewed in conjunction with a popular model of color
erties of pigments derived from the four families is shown in Figure 1. discrimination Chiao et al. (2000) examined how photo-
All four gene families are believed to have arisen early in vertebrate pigment spectral positioning might influence color
evolution. The Rh2 gene family is not present in any contemporary discrimination. For pigment combinations involving
mammals and so is presumed to have been lost during the early
short-wavelength pigments with kmax >400 nm, varia-
evolution of mammals. The distribution of the extant gene families
among the three groups of contemporary mammals is given at the tions in the positioning of the LWS pigment from its
top; SWS1 is a pseudogene in present-day monotremes. Repre- longest to its shortest position had only very modest
sentation of the SWS2 gene family was lost prior to the divergence of effects on predicted discriminability. From their com-
marsupial and eutherian mammals. (Modified from Jacobs, 2009). putations these authors additionally inferred that color
discrimination in such dichromats could be maximized
et al., 2008). These cone pigments (bottom of Figure 1) by increasing the spectral separation between the two
represent the shortest and longest spectral positions that pigments, irrespective of the nature of the visual
can be generated from cone opsins linked to a retinal-1 environment. Modeling analyses such as this one thus
chromophore and would have provided the photopig- provide no obvious explanation for the significant
ment potential for dichromatic color vision. variations in the position of the LWS pigment across
these dichromatic mammals. One possibility is that in
such cases the spectral tuning of the LWS pigment has
Spectral positioning of mammalian cone pigments
been more impacted by the demands of those capacities
Since all mammalian photopigments are constructed supported by achromatic vision (Chiao et al., 2000;
from the same chromophore, retinal-1, variations in Osorio and Vorobyev, 2005). Another is that, within
their spectral absorption properties must be due to opsin some fairly broad limits, pigment positioning is not
variations. Molecular genetic studies show that varia- critically important for supporting visual needs; that
tions at a limited number of positions in the opsin rather the observed variations seen among mammals
molecule are largely responsible for all the variations in better reflect events that occurred in the earlier history
the spectral positioning of photopigments. In the case of of the various animal groups, than it does in matching
mammalian LWS pigments, for example, dimorphic current visual demands. This latter scenario merits
variations at only five amino acid sites cause variations attention because it at least seems to provide the best
in pigment spectral positioning, with combinations of explanation for variations in photopigment positioning
changes occurring at these critical sites allowing for the in many insects (Briscoe and Chittka, 2001).
production of pigments occupying quite a number of
possible spectral positions (Yokoyama and Radlwim-
The primate story
mer, 2001). Mutagenesis studies show that four amino
acid positions can potentially influence the spectral Primates have long been known to constitute a special
tuning of the primate LWS pigments (Asenjo et al., case, but it is only in recent years that a fuller
1994), with only three of these accounting pretty well for appreciation of the diversity of primate color vision
ª 2010 The Author, Ophthalmic and Physiological Optics ª 2010 The College of Optometrists428 Ophthal. Physiol. Opt. 2010 30: No. 5
emerged, and along with it a more detailed understand- most of the other contemporary platyrrhines (Kainz
ing of its evolution. In large part these changes were et al., 1998; Dulai et al., 1999).
fostered by studies of the cone opsin genes and cone The third group of primates, the strepsirrhines, is
photopigments in many different primates. Several usually described as more primitive. Animals of this
recent reviews may be consulted for access to what is group feature afoveate, more rod-dominated, retinas
now an extensive literature on this topic (Regan et al., and their eyes often contain a tapetum. To date these
2001; Osorio et al., 2004; Jacobs, 2007, 2008). primates have been less well studied, but they too show
Although the idea is not without its critics (e. g., Tan significant variations in their cone photopigment com-
et al., 2005), it is usually believed that the earliest plements. Three principal variants have been identified.
primates were nocturnal, and thus like most eutherian Two of these have been described above—some are like
mammals probably had two types of cone pigment the bushbaby (Otolemur) in having only a single type of
drawn, respectively, from the SWS1 and LWS opsin cone pigment and thus lacking color vision; while others
gene families. In mammals the LWS cone opsin genes resemble the ring-tailed lemur (Lemur catta), and many
are located on the X-chromosome, but, unlike other other mammals, in having two types of cone pigment and
mammals, catarrhine primates (Old World monkeys, dichromatic color vision (Kawamura and Kubotera,
apes and humans) have two different LWS genes that 2004). In a third variant, some species from this group
specify cone photopigments with peaks at about 530 nm have polymorphic X-chromosome opsin genes and thus,
and 560 nm (commonly called M and L respectively). similar to the platyrrhines, have the photopigment basis
Since these two are effectively conserved across all the to support a mixture of dichromatic and trichromatic
catarrhines they apparently emerged as a consequence of phenotypes (Tan and Li, 1999; Jacobs et al., 2002;
a gene duplication that occurred close to the base of the Velleux and Bolnick, 2009). An understanding of the
catarrhine radiation, some 30–40 mya (Nathans et al., evolution of opsin genes and color vision in this group
1986). In conjunction with the pigment product of an of primates remains very much a goal for future studies.
autosomal SWS1 gene, all of the species of this group The production of color vision requires, as a mini-
express three classes of cone photopigment and have mum, multiple types of receptor containing different
trichromatic color vision. Thus catarrhine primates, photopigments and a nervous system capable of con-
alone among eutherian mammals, have been able to add trasting the pattern of photon absorption in the different
a second version of an LWS gene and exploit its pigment types of photoreceptor. Two such neural arrangements
product to acquire a new dimension of color vision. are generally believed to characterize mammalian reti-
The other large group of anthropoid primates, the nas (Lee, 2004; Wässle, 2004). One involves a dedicated
New World platyrrhine monkeys, has highly diverse class of bipolar cells (the S-cone bipolars) that selectively
color vision and, as a consequence, has been much contact short-wavelength cones. Signals from these
studied in recent years (Jacobs, 2007). With only two cones are fed via S-cone bipolar cells to a class of small
apparent exceptions, this entire group features X-chro- bi-stratified ganglion cells that also receive antagonistic
mosome opsin gene polymorphisms, the most common inputs from a group of bipolar cells that contact M/L
arrangement featuring three alternate forms of the LWS cones. The combination of these inputs provides the
gene with each allele specifying a photopigment with basis for a spectrally-opponent pathway that can sup-
kmax in the 530–562 nm range. As a consequence of port a dimension of color vision. Although the compar-
early X-chromosome inactivation, heterozygous females ative evidence is still somewhat scanty, it seems likely
express two types of M/L pigment and derive trichro- that this neural pathway is characteristic of the retinas
matic color vision while homozygous females and all of all eutherian mammals and thus has been conserved
males have a single M/L pigment and are dichromatic. throughout the history of this group. The other circuit
This arrangement yields a total of six distinct color for extracting color information is unique to primate
vision phenotypes. The two exceptions are Aotus, which retinas. It originates from the M or L cone inputs to
has only a single LWS pigment and thus lacks conven- midget bipolar cells which in turn synapse on midget
tional color vision (above), and the howler monkey ganglion cells where that signal is combined in opponent
Alouatta which resembles the catarrhine norm in having fashion with signals originating from neighboring M or
two populations of M/L cone pigments (Jacobs et al., L cones. These form the substrate for the second
1996a) and being uniformly trichromatic (Araujo et al., spectrally-opponent channel, setting the stage for an
2008). Evidence suggests that the addition of a second additional dimension of color vision (Martin, 1998). The
X-chromosome opsin gene in the howler monkey midget cell pathway has been identified as being present
occurred independently from the gene addition that in retinas of a number of disparate primate species, even
occurred in the catarrhine primates; in the case of those lacking trichromatic color vision, and so is
howler monkeys probably emerging against a back- believed to have appeared early in primate evolution
ground of earlier polymorphisms similar to that seen in (Silveira et al., 2005). There remains lively debate as to
ª 2010 The Author, Ophthalmic and Physiological Optics ª 2010 The College of OptometristsThe Verriest Lecture: G. H. Jacobs 429
the nature of spatial arrangements of L and M cone Mollon, 2000; Dominy and Lucas, 2001; Regan et al.,
signals to this second pathway (Solomon and Lennie, 2001; Parraga et al., 2002).
2007) and of the function(s) that this pathway may have With their dramatic individual variations in color
subserved in primates prior to the points at which a vision platyrrhine monkeys provide a rich resource for
second type of M/L cone appeared (Mollon, 1989; Lee, examining the linkages between color vision capacity
2004), and behavior. Since there is evidence that the M/L cone
Recent years have seen a marked increase in the pigments of the platyrrhines have been under selection
number of studies asking how well suited the various for a considerable period of time (Surridge et al., 2003),
forms of primate color vision are for various life- one might confidently expect to find among these
supporting visual behaviors and, by extension, perhaps monkeys individual differences in behavior that corre-
thereby shedding some light on the circumstances that late with individual differences in color vision. Exper-
led to the evolution of the mechanisms underlying color iments conducted in laboratory settings have in fact
vision. Such investigations typically start with detailed detected some differences in foraging efficiency for
measurements of natural spectral environments and monkeys of different phenotypes (Caine and Mundy,
then use one or other of the computational models of 2000; Smith et al., 2003); however, studies of several
visual processing to predict discriminative performance. different platyrrhine species in their natural habitats
These exercises show consistently that the discrimina- have so far proven singularly unsuccessful in detecting
tion capacities inherent in primate trichromacy are well individual variations in behavior that can be compel-
suited to support the demands of foraging, whether the lingly traced to individual variations in color vision
targets are edible fruits or foliage viewed in their natural (Dominy et al., 2003; Smith et al., 2003; Vogel et al.,
surrounds (Osorio and Vorobyev, 1996; Sumner and 2007; Hiramatsu et al., 2008; Bunce, 2009). Why this
Table 1. Recent laboratory investigations of mammalian color vision
Exemplars
Order (Genus, common name) Goal of study* Reference
Marsupalia Macropus (wallaby) Dichromacy Hemmi, 1999
Sminthopsis (dunnart) Trichromacy Arrese et al., 2006
Rodentia Mus (mouse) Dichromacy Jacobs et al., 2004
Rattus (rat) Dichromacy Jacobs et al., 2001
Cavia (guinea pig) Dichromacy Jacobs and Deegan,1994b
Meriones (gerbil) Dichromacy Jacobs and Deegan, 1994a
Spermophilus (ground squirrel) Color thresholds van Arsdel and Loop, 2004
Primate Alouatta (howler monkey) Trichromacy Araujo et al., 2008
Callithrix (marmoset) Distinctiveness of color Derrington et al., 2002
Callithrix (marmoset) Polymorphism Pessoa et al., 2005a
Cebus (capuchin monkey) Stimulus size and color vision Gomes et al., 2005
Eulemur (black lemur) Presence of color vision Gosset and Roeder, 2000
Leontopithecus (golden lion) Polymorphism Pessoa et al., 2005b
Pan (chimpanzee) Color classification Matsuno et al., 2004
Papio (baboon) Color categorization Fagot et al., 2006
Saguinus (tamarin) Polymorphism Pessoa et al., 2003
Scandentia Tupaia (tree shrew) Color thresholds van Arsdel and Loop, 2004
Cetacea Tursiops (dolphin) Rod contributions to color Griebel and Schmid, 2002
Artiodactyla Bos (cow) Dichromacy Phillips and Lomas, 2001
Dama (fallow deer) Presence of color vision Birgersson et al., 2001
Perissodactyla Equus (horse) Dichromacy Pick et al., 1994
Dichromacy Macuda and Timney, 1999
Dichromacy Smith and Goldman, 1999
Dichromacy Geisbauer et al., 2004
Dichromacy Hanggi et al., 2007
Dichromacy Ahmadinejad et al., 2008
Color Thresholds Roth et al., 2008
Carnivora Felis (cat) Presence of color vision Tritsch, 1993
Color thresholds Tritsch, 1995
Sirenia Trichechus (manatee) Dichromacy Griebel and Schmid, 1996
*The meanings of the comments are explained in the text.
ª 2010 The Author, Ophthalmic and Physiological Optics ª 2010 The College of Optometrists430 Ophthal. Physiol. Opt. 2010 30: No. 5
should be so is puzzling and remains under active
Conclusion
investigation.
Recent progress toward gaining a more complete picture
of mammalian color vision can be largely attributed to
Laboratory investigations of mammalian color vision
technical advances in molecular genetics, cell biology,
A large majority of the publications on the topic of and electrophysiology, each of which has significantly
mammalian color vision produced over the past expanded our understanding of the current picture of
15 years, including most of those referenced above, deal the distribution of cone pigments across extant mam-
not with color vision but with various biological mals, of what these pigments predict about color vision,
mechanisms linked to that capacity. There are probably and of how these arrangements may have evolved. For
at least two factors that have contributed to this reasons noted above, progress in the challenging task of
imbalance. For one thing, behavioral studies of color measuring color vision in non-human subjects has been
vision in non-human species are especially challenging slower, while a detailed understanding of how various
and time consuming relative to studies of mechanisms, animals employ color vision in support of their survival
often taking months, even years, to complete. A second remains largely a task for the future. Finally, recent
impediment is that in current times funding agencies experiments have opened the door to actively manipu-
have show only modest inclination to support such lating color vision either through direct alterations of
ventures. Despite these challenges, there have neverthe- the opsin gene complement (Jacobs et al., 2007) or by
less been a number of investigations that posed direct changes in the photopigment array induced by a gene
questions about color vision in various mammals. transfer paradigm (Mancuso et al., 2009). Such proce-
Reports from such studies that have come to my dures hold the promise of allowing direct tests of
attention are listed in Table 1. hypotheses about the evolution of color vision as well as
Space does not permit extended discussion of these more searching examinations of various aspects of the
investigations of mammalian color vision. Instead, a neural underpinnings of color vision.
summary comment is offered for each in Table 1. A
number of these studies sought to establish the dimen-
Acknowledgements
sionality of color vision in some target species. These
(indicated as ÔDichromacyÕ or ÔTrichromacyÕ depending I thank the officers and members of the International
on the results claimed) involved tests using either spectral Colour Vision Society for providing the opportunity to
lights or calibrated colored papers as test stimuli. The present the Verriest lecture at their 2009 meeting in
trichromatic color vision found in the marsupial Sminth- Braga, Portugal.
opsis (the dunnart) is particularly noteworthy because
that species expresses only two different cone opsins, the
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